Quorum Sensing Modulates the Epibiotic-Parasitic Relationship Between Actinomyces odontolyticus and Its Saccharibacteria epibiont, a Nanosynbacter lyticus Strain, TM7x

Joseph K Bedree; Batbileg Bor; Lujia Cen; Anna Edlund; Renate Lux; Jeffrey S McLean; Wenyuan Shi; Xuesong He

doi:10.3389/fmicb.2018.02049

Quorum Sensing Modulates the Epibiotic-Parasitic Relationship Between Actinomyces odontolyticus and Its Saccharibacteria epibiont, a Nanosynbacter lyticus Strain, TM7x

Front Microbiol. 2018 Sep 24:9:2049. doi: 10.3389/fmicb.2018.02049. eCollection 2018.

Authors

Joseph K Bedree^{1

2}, Batbileg Bor², Lujia Cen², Anna Edlund³, Renate Lux⁴, Jeffrey S McLean⁵, Wenyuan Shi², Xuesong He²

Affiliations

¹ Section of Oral Biology, Division of Oral Biology and Medicine, School of Dentistry, University of California, Los Angeles, Los Angeles, CA, United States.
² Department of Microbiology, The Forsyth Institute, Cambridge, MA, United States.
³ Department of Genomic Medicine, J. Craig Venter Institute, La Jolla, CA, United States.
⁴ Section of Periodontics, Division of Constitutive and Regenerative Sciences, School of Dentistry, University of California, Los Angeles, Los Angeles, CA, United States.
⁵ Department of Periodontics, School of Dentistry, University of Washington, Seattle, WA, United States.

Abstract

The ultra-small, obligate parasitic epibiont, TM7x, the first and only current member of the long-elusive Saccharibacteria (formerly the TM7 phylum) phylum to be cultivated, was isolated in co-culture with its bacterial host, Actinomyces odontolyticus subspecies actinosynbacter, XH001. Initial phenotypic characterization of the TM7x-associated XH001 co-culture revealed enhanced biofilm formation in the presence of TM7x compared to XH001 as monoculture. Genomic analysis and previously published transcriptomic profiling of XH001 also revealed the presence of a putative AI-2 quorum sensing (QS) operon, which was highly upregulated upon association of TM7x with XH001. This analysis revealed that the most highly induced gene in XH001 was an lsrB ortholog, which encodes a putative periplasmic binding protein for the auto inducer (AI)-2 QS signaling molecule. Further genomic analyses suggested the lsrB operon in XH001 is a putative hybrid AI-2/ribose transport operon as well as the existence of a luxS ortholog, which encodes the AI-2 synthase. In this study, the potential role of AI-2 QS in the epibiotic-parasitic relationship between XH001 and TM7x in the context of biofilm formation was investigated. A genetic system for XH001 was developed to generate lsrB and luxS gene deletion mutants in XH001. Phenotypic characterization demonstrated that deletion mutations in either lsrB or luxS did not affect XH001's growth dynamic, mono-species biofilm formation capability, nor its ability to associate with TM7x. TM7x association with XH001 induced lsrB gene expression in a luxS-dependent manner. Intriguingly, unlike wild type XH001, which displayed significantly increased biofilm formation upon establishing the epibiotic-parasitic relationship with TM7x, XH001ΔlsrB, and XH001ΔluxS mutants failed to achieve enhanced biofilm formation when associated with TM7x. In conclusion, we demonstrated a significant role for AI-2 QS in modulating dual-species biofilm formation when XH001 and TM7x establish their epibiotic-parasitic relationship.

Keywords: Actinomyces; TM7; epibiont; human-associated; interspecies interaction; oral microbiome.

Abstract

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